Biosaintifika 12 (1) (2020): 70-75 p-ISSN 2085-191X | e-ISSN 2338-7610

Journal of Biology & Biology Education https://journal.unnes.ac.id/nju/index.php/biosaintifika

Tyrosinase Inhibition, Antiglycation, and Antioxidant Activity

of Xylocarpus granatum
Irmanida Batubara1,2*, Maily3, Wulan Tri Wahyuni1,2, Kilala Tilaar3, Waras Nurcholis2,4,
Fransiska Devi Junardy3, Yogo Suro Priyadi3, Erna Martina Subroto3, Saat Egra5,
Nevianti Zamany2,6
1
Department of Chemistry, Faculty of Mathematics and Natural Sciences, IPB University, Bogor, Indonesia
2
Tropical Biopharmaca Research Center, IPB University, Bogor, Indonesia
3
PT Martina Berto, Jakarta, Indonesia
4
Department of Biochemistry, Faculty of Mathematics and Natural Sciences, IPB University, Bogor, Indonesia
5
Faculty of Agriculture, University of Borneo Tarakan, North Kalimantan, Indonesia
6
Faculty of Fisheries and Marine Science, IPB University, Bogor, Indonesia
*Email: ime@apps.ipb.ac.id

Submitted: 26 Desember 2019. Revised: 11 February 2020. Accepted: 20 March 2020

Abstract. Xylocarpus granatum is mangrove plant that traditionally used as face powder in Central Sulawesi, Indonesia which related to
antioxidant, antiglycation and tyrosinase inhibition activities. This study aimed to evaluate the potency of X. granatum as a tyrosinase
inhibitor, antiglycation, and antioxidant. The leaves, stem, stem bark, fruit flesh, fruit peel, and kernel of X. granatum were extracted
using ethanol, then their tyrosinase inhibition, antiglycation, and antioxidant were evaluated. Tyrosinase inhibition activity was evaluat-
ed using in vitro assay with L-tyrosine and L-DOPA as the substrate of monophenolase and diphenolase. Antiglycation activity was
studied by measuring the excitation and emission fluorescence from glucose and fructose reaction with Bovine Serum Albumin. Antiox-
idant activity was measured using the DPPH radical scavenging assay. The result showed that the ethanolic extract of fruit flesh has
higher potency as a tyrosinase inhibitor (IC50 of 393.8 mg/L and IC50 of 448 mg/L, respectively for monophenolase and diphenolase).
Antiglycation assay showed that the ethanolic extract of stem bark provides the strongest antiglycation activity with an IC50 of 118.1
mg/L. Meanwhile, fruit peel provides the strongest antioxidant activity with an IC50 of 5.5 mg/L. Fractionation of ethanolic extracts of
each part of X. granatum tree yield fractions with lower bioactivity compared to the crude extract. Moreover, stem extract and fractions
from two different locations (Tarakan and Kendari) tend to have different bioactivities strengths. The stem part of X granatum could be
developed as a new raw material of cosmetic products in Indonesia, while ethanol as the solvent for extraction and the different bioactiv-
ity of stem extract from a different location can be the consideration for the industry to standardize the extract prior to production of the
final product.

Keywords: Antiglycation, Antioxidant, Tyrosinase inhibition, Xylocarpus granatum

How to Cite: Batubara, I., Mustofa, M., Wahyuni, W. T., Tilaar, K., Nurcholis, W., Junardy, F. D., ... & Zamany, N. (2020). Tyrosinase
Inhibition, Antiglycation, and Antioxidant Activity of Xylocarpus granatum. Biosaintifika: Journal of Biology & Biology Education, 12
(1), 70-75

DOI: http://dx.doi.org/10.15294/biosaintifika.v12i1.22676

INTRODUCTION idant and tyrosinase inhibition activity (Zamani et al.,

Xylocarpus granatum is a mangrove species grows
in the upper intertidal zone of mangrove forests and
native to Tropical mangrove forests (Allen et al.,
2003). This mangrove species is widely used by the
local community as traditional medicinal plants, while
the wood of this plant is used to make boats and furni-
ture. Previous research reported that bark of X. gran-
atum has the potency as anti-diarrhea, anti-bacterial,
anti-diabetic, lipase inhibition, and antioxidant
(Markers, 1972; De Bruyne et al., 1999; Scalbert,
1991; Veluri et al., 2004; Batubara et al. 2009, Das et
al., 2019). Active compounds of X. granatum fruit
possess a significant antisecretory effect on peptic
ulcers (Lakshmi et al., 2010). Another study reported
that the extract of X. granatum seed kernel has antiox-
2015).
Besides being used as a medicinal plant, X. gran-
atum (especially its fruit) is used by the local commu-
nity of Togean Island, Central Sulawesi, Indonesia as
a facial mask for the bride. Based on that local
knowledge, the potency of X. granatum as a cosmetic
ingredient and personal care is an interesting aspect to
be explored. In tropical countries with high intensity
of sunshine throughout the year, cosmetics and per-
sonal care with lightening activities are very popular.
Furthermore, cosmetics that appeal to women are
ones with antiaging activity. On the other hand, cos-
metics that contain antioxidants are also needed be-
cause it can protect the skin from the radical species
that cause damage to the skin.
The research purposes was to evaluate the potency
of X, granatum as a lightening, anti-aging, and antiox-

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idant agent using a different part of X. granatum, the
different solvent of extraction/fractionation, and dif-
ferent growth location. The information about the
most effective part of the plant to be used for cosmet-
ics purposes, the best solvent for extraction, and the
quality of raw material from a different location, will
be scientific evidence to develop the new cosmetic
product in Indonesia as well as to standardize the
product.
METHODS
X. granatum was collected from Tarakan, North
Kalimantan and Kendari, Southeast Sulawesi, Indone-
sia. Chemical reagents such as 2,2’-diphenylpicryl
hydrazyl (DPPH), ethanol, L-tyrosine, L-DOPA, tyro-
sinase, methanol, ethyl acetate, n-hexane, bovine se-
rum albumin (BSA), glucose, fructose, ascorbate acid,
dimethyl sulphoxide (DMSO) were purchased from
SIGMA Aldrich and Merck and used without any
purification. ELISA plate well reader (Merk Biotek
Epoc Spektro UV-Vis) was used for antioxidant and
tyrosinase inhibition assay, while fluorometer
(FluoroStar BMG Labtech) was used for antiglycation
assay.
Sample Preparation, Extraction, and Fractiona-
tion
The sample was separated into several parts,
namely leaves, stem, stem bark, fruit flesh, fruit peel,
and kernel. Each part of the sample was washed and
dried in the oven at a temperature of 40-60 °C. The
dried sample was ground to obtain sample powder
with an average size of 20 mesh prior to the extraction
process. Ethanol was used as the solvent in the mac-
eration extraction of the samples. The crude ethanolic
extracts were then dried using a rotary evaporator
prior to use in the bioactivity test. Liquid-liquid frac-
tionation was conducted using n-hexane and ethyl
acetate to the ethanolic extract to obtain fractions with
different polarities.
Tyrosinase Inhibitory Assay
Tyrosinase inhibitory activity was evaluated based
on inhibition of the sample to monophenolase and
diphenolase activity. The assay was carried out using
L-tyrosine and L-DOPA as the substrates, following
the method as described by Batubara et al. (2010).
Kojic acid was used as a positive control.
Antiglycation Assay
Antiglycation activity was evaluated according to
the Povichit et al. (2010) method with modification as
71
mention by Zahra et al. (2016). Aminoguanidine was
applied as a positive control.
Antioxidant Assay
Antioxidant activity was evaluated based on
DPPH radical scavenging activity, following Batubara
et al. (2009) with modification. The amount of 100
µL DPPH solution 125 µM was mixed with 100 µL
of the sample in various concentrations. The mixture
was then incubated at 37 °C for 30 minutes. The ab-
sorbance of the sample was measured at 517 nm. Eth-
anol was used as solvent and blank, while ascorbic
acid was used as positive control.
Inhibition (%) =
Where,
Asample: Absorbance of the sample
Acontrol: Absorbance of ascorbic acid as the positive
control
Ablank: Absorbance of ethanol as the blank
Statistical Analysis
The data resulted in this study was performed in
triplicate and reported in the average. T-test was used
for evaluating the activity data obtained using two
ways ANOVA, followed by Duncan multiple compar-
ison tests.
RESULTS AND DISCUSSION
As described before, the fruit of X. granatum is
empirically used by the local coastal community for
facial mask, and it is believed to be able to enhance
the woman’s beauty. Zamani et al. (2015) reported
that fruit peel of X. granatum has antioxidant and
tyrosinase inhibitory activity, thus make this plant is
prospective to be utilized as an active ingredient of
cosmetic. Otherwise, the amount of fruit that can be
collected from X. granatum tree is limited. Therefore,
the investigation to evaluate the potency of other parts
of X. granatum as active ingredients of cosmetics is
needed. We selected the aerial part, including leaf that
is available every time, stem (including the twig), and
fruits. The fruit was also divided into three parts i.e.,
fruit peel, fruit flesh, and kernel. In this study, the
leaves, stem, stem bark, fruit flesh, fruit peel, and
kernel of X. granatum (Figure 1) were evaluated for
their tyrosinase inhibition activity, antiglycation, and
antioxidants activity.
 Ferymon Mahulette et al. / Biosaintifika 12 (1) (2020): 70-75

(a) (b)
Figure 1. Xylocarpus granatum and its parts, stem, leaf, fruit (a) and its fruit with the part: fruit peel, fruit flesh
(seed coat), and seed kernel (b)

Table 1. Tyrosinase inhibitory, antiglycation, and antioxidant activity of ethanolic extract of the different part
of X. granatum
Tyrosinase inhibitory activity (IC50, mg/L) Antioxidant
Ethanolic extract of Antiglycation (IC50, mg/L) (IC50,
Monophenolase Diphenolase mg/L)
d f e
Leaves >12500 >12500 >500 253.3g
c d b
Stem 885.4 2150.0 125.9 6.8c
Stem Bark 394.4b 1792.3c 118.1b 12.0f
Fruit flesh 393.8b 448.0b 447.9d 8.9d
Fruit peel 417.0b 3340.7e 309.1c 5.5b
b d e
Kernel 447.1 2330.0 >500 10.8e
Ascorbic acid N.A N.A N.A 3.5a
Kojic acid 46.1a 78.3a N.A N.A
a
Aminoguanidine N.A N.A 20.11 N.A
N.A: Not applicable; Data followed by the same letter in the same column are not significantly different ac-
cording to Duncans multiple comparison test (P<0.05).

Tyrosinase inhibitory activity was evaluated to
measure the ability of samples as lightening agents.
Tyrosinase inhibition is correlated with the decrease
of melanogenesis on the skin since this enzyme is
responsible for melanogenesis or hyperpigmentation
in mammals, including humans (Chang, 2009). Tyro-
sinase activity was evaluated using two types of sub-
strate, namely L-tyrosine (evaluate the activity of
monophenolase) and L-DOPA (evaluate the activity
of diphenolase). Investigation of tyrosinase inhibitory
activity showed that fruit flesh of X. granatum pos-
sess higher inhibitory activity against tyrosinase (IC50
of 448 and 394 mg/L, respectively for L-tyrosine and
L-DOPA) compared to the other parts of the plant,
even though its inhibitory activity is lower than kojic
acid (positive control). The activity of the fruit flesh is
not significantly different compared with stem bark,
fruit-peel, and kernel extract on monophenolase reac-
tion but significantly different on diphenolase reac-
tion. On the other word, the other parts of X. gran-
atum plant that shows tyrosinase inhibitory activity
for the L-tyrosine substrate are stem, stem bark, fruit
peel, and kernel (Table 1). Batubara et al. (2010) re-
ported that some Indonesian medicinal plants, includ-
ing X. granatum has the potency as an inhibitor of
tyrosinase.
The potency of X. granatum extract as an anti-
aging agent was evaluated through antiglycation as-
say. Glycation is a reaction between free reducing
sugars with free amino groups of proteins, DNA, and
lipids. This spontaneous reaction leads to the for-
mation of advanced glycation end products (AGEs)
(Kim et al., 2017) and furthermore lead to a loss of
protein function and impaired elasticity of tissues,
including skin and associated with promoting aging
(Semba et al., 2010; Nguyen & Katta, 2015). Anti-
glycation activity assay shows that the ethanolic ex-
tract of stem and stem bark of X. granatum have po-
tency as an antiglycation agent (IC50 of 118 and 126
mg/L, respectively), but not as good as aminoguani-

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 Ferymon Mahulette et al. / Biosaintifika 12 (1) (2020): 70-75
dine as a positive control. This result agrees with the
report of Sapitri et al. (2019) that claimed that the
stem of X. granatum has antiglycation activity. The
next prospective extract is fruit peel extract that is
also had antiglycation activity (Table 1).
Reactive Oxygen Species (ROS) enhance melanin
biosynthesis, induce proliferation of melanocytes
(Yasui & Sakurai, 2003), and plays an important role
in AGEs formation and accumulation which leads to
pathogenesis of skin (Yamakoshi et al., 2003). There-
fore, antioxidant activity is an important aspects relat-
ed to skin health and skin protection. In this study, the
antioxidant activity of X. granatum extract and frac-
tion were evaluated by DPPH radical scavenging
activity assay. The result shows that all of ethanolic
extracts from all part of X. granatum (stem, stem
bark, fruit peel, fruit flesh, and kernel) has big poten-
cy as antioxidant agents. Strongest antioxidant activi-
ty was performed by fruit peel and stem with IC50 of
5.5 and 6.8 mg/L, respectively, while IC50 of ascorbic
acid as a positive control was 3.5 mg/L (Table 1).
Based on the three in vitro assay determination on
this study, the most prospective parts are stem and
fruit-peel. Stem and fruit-peel have a high tyrosinase
inhibition activity on monophenolase, high anti-
glycation activity, and high antioxidant activity. Fruit-
peel can be utilized as cosmetic raw materials because
this part is not used for generative purposes, only the
seed kernel and seed coat is important for generative
purposes. The fruit is not available all year, so it is
more reasonable to select the stem part to be devel-
oped as a new cosmetic product. These results also
suggest not selecting the main stem as cosmetic raw
materials, but the small stem such as twig can be
used. By using a small stem, it will conserve the
plant. By pruning process of X. granatum, the farmer
could collect the twig or branch and use it as cosmetic
raw materials.
In order to select the best solvent to be used to
prepare the cosmetic product, the fractionation of
ethanolic extract was performed. Fractionation of
ethanolic extract of leaves, bark, fruit peel, and stem
was carried out using n-hexane and ethyl acetate.
Evaluation of tyrosinase inhibitory activity,
antiglycation activity, and antioxidant activity were
also conducted to each fraction. The results showed
that bioactivities of n-hexane, ethyl acetate, and
73
residual ethanol fraction are lower compared to its
crude ethanolic extract (Table 2). The antioxidant
activity that gives a higher activity after fractionation
was found on the stem-bark extract. The first ethanol-
ic extract of stem bark has IC50 of 12.0 mg/L (Table
1), and after fractionation, the activity is higher such
as shown on the ethyl acetate fraction with IC50 of 4.2
mg/L (Table 2). For the antiglycation activity, the
increasing activity after fractionation is found on
fruit-peel extract (IC50 309.1 mg/L before fractiona-
tion and after fractionation on ethyl acetate and resid-
ual ethanol has lower IC50 of 103.0 mg/L and 166.0
mg/L, respectively). The results indicated that active
constituents in ethanolic extract probably
synergistically provide the bioactivities, although this
assumption needs to be further proven. These results
suggest to use only ethanol as the solvent for extrac-
tion of X. granatum for cosmetic raw materials, and
further separation to find active ingredient is better
using ethyl acetate for fractionation.
On the basis of the bioactivities of each extract of
X. granatum parts and considering the amount of the
extract; thus comparison of the bioactivities of the
stem extract and fractions collected from two differ-
ent areas (Tarakan, North Kalimantan and Kendari,
Southeast Sulawesi, Indonesia) were carried out. The
results indicated that ethanolic extract of X. granatum
stem from Kendari provide stronger antioxidant com-
pared to the sample from Tarakan, except for its n-
hexane fraction. Tyrosinase inhibition of X. granatum
stem from Kendari also tend to be stronger (for L-
tyrosinase substrate) compared to that from Tarakan.
Meanwhile, tyrosinase inhibition (for L-DOPA sub-
strate) of both samples are comparable (Table 3).
From these results, we can state that the origin of the
X. granatum could influence its bioactivities; this may
be due to the difference in environmental conditions.
Based on this research results, it is found that the
most prospective parts of X. granatum that could be
developed as cosmetic raw materials is stem/twig and
fruit-peel. As cosmetics raw material, ethanol can be
used as a solvent for extraction, and it is not important
to separate further. The industry that will use this
material as cosmetics raw materials needs to consider
the origin of plants and standardize it to make sure the
quality, safety, and efficacy of the product.
 Ferymon Mahulette et al. / Biosaintifika 12 (1) (2020): 70-75

Table 2. Tyrosinase inhibitory, antiglycation, and antioxidant activity of fractions of ethanolic extract of the
different part of X. granatum
Tyrosinase inhibitory activity
Fraction (IC50, mg/L) Antiglycation
Sample Antioxidant
(IC50, mg/L)
Monophenolase Diphenolase (IC50, mg/L)
Leaves n-Hexane 8017.4i 3403.7f >500g >500i
j k g
Ethyl acetate >12500 >12500 >500 >500i
Residual ethanol >12500j 11992.2j >500g 303.8h
Stem Hexane 1469.0g 9272.0i >500g 26.9f
Ethyl acetate 444.6b 665.9c 160.6c 53.5g
h b d
Residual ethanol 2083.4 578.7 232.2 18.6e
Stem Bark n-Hexane 1343.7f 8587.1h >500g 27.9f
Ethyl acetate 1217.4e 2962.2e 245.6e 4.2b
Residual ethanol 628.5c 1262.2d 245.7e 12.5d
h g f
Fruit peel n-Hexane 2081.2 4311.2 398.6 56.5g
Ethyl acetate 1149.1d 706.5c 103.0b 8.4c
Residual ethanol 1454.1g 3395.2f 166.9c 11.3d
Ascorbic acid N.A N.A N.A 3.5a
a a
Kojic acid 46.1 78.3 N.A N.A
a
Amoniguanidine N.A N.A 20.11 N.A
N.A: Not applicable; Data followed by the same letter in the same column are not significantly different ac-
cording to Duncans multiple comparison test. P<0.05

Table 3. Tyrosinase inhibition and antioxidant activity of extract and fraction of X. granatum stem from Ken-
dari
Origin Antioxidant Antityrosinase Activi- Antityrosinase Activities
of Sam- Stem of X. granatum Activities (IC50, ties with L-tyrosine as with L-Dopa as Substrate
ples mg/L) Substrate (IC50, mg/L) (IC50, mg/L)
Kendari Ethanolic crude extract 3.2a 512.0d 609.3b
n-Hexane fraction 216.4b >1000e >1000e
Ethyl acetate fraction 3.2a 355.4c 882.7c
Residual ethanol fraction 3.4a 291.6b 957.4d
Ascorbic acid 2.8a N.A N.A
Kojic acid N.A 39.7a 65.5a
N.A: Not applicable; Data followed by the same letter in the same column are not significantly different ac-
cording to Duncans multiple comparison test. P<0.05

CONCLUSION ACKNOWLEDGMENTS

X. granatum has a potency to be utilized as an ac-
tive ingredient of cosmetics and personal care since it
provides tyrosinase inhibitory, antiglycation, and
antioxidant activity. Part of X. granatum tree that
performs higher tyrosinase inhibition activity is fruit
flesh. However, the stem of X. granatum provides
higher antioxidant and antiglycation bioactivities, and
this part of X. granatum tree has higher availability
compared to the other parts of the plant. Fractionation
of ethanolic extract of each part of X. granatum tree
does not provide fraction with higher bioactivities.
Meanwhile, stem extract and fractions from different
areas tend to have different bioactivity strengths.
74
Authors would like to acknowledge The Ministry
of Research, Technology, and Higher Education for
funding the Program Insentif Riset Pengembangan
Teknologi Industri Contract No. 16/GI/PPK/E/E4/
2019
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